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Zebra finch study finds mixed impact of early-life stress

When male zebra finches were stressed early in life, they wound up with duller beaks but sang more complex songs.

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A bout of early-life stress can have lifelong impacts on two key signals that help male zebra finches attract mates: beak color and song complexity. But rather than being uniformly negative, a recent study published in Functional Ecology found that the consequences of stress are mixed. Stressed males wind up with duller, less colorful beaks but sing more complex songs.

“That caught us totally off guard,” said Loren Merrill, a postdoctoral researcher at the Illinois Natural History Survey who was lead author on the study conducted with principal investigator Jennifer Grindstaff, an associate professor at Oklahoma State University. Previous studies found that challenges like infection or lack of nutritious food early in life could lead to poorer outcomes for adult birds, so the team expected that when they activated the young males’ immune systems by treating them with an antigen, those birds would sing less complex songs later in life.

“That’s what we saw with beak coloration,” Merrill said. The males treated with KLH (keyhole limpet hemocyanin, a molecule that stimulates an immune response) “had duller, less colorful beaks, and that impact lasted throughout their lives.”

While beak color can fluctuate throughout a bird’s life based on diet and health, for a KLH-treated bird “the upper limit of his coloration seems to be set in that early-life period. There’s sort of a cap on how ‘sexy’ or red his beak can be,” Merrill said.

“Beak coloration has been linked to attractiveness, but it’s not clear whether females actually prefer males with brighter red bills, or whether that co-varies with other characteristics, like song complexity. Both reflect an individual in good condition,” Merrill said. “Beak coloration may be more important as a signal to other males, as a sign of dominance and competitive ability.” Rather than appealing directly to female zebra finches, beak color may influence the hierarchy among males, and that hierarchy in turn may affect which males the females choose as mates.

Female zebra finches also assess song quality when choosing mates. Each male typically produces one song that is composed of different elements. Each element can be unique, or a male can recycle an element and use it multiple times; they also can combine elements into phrases. Scientists believe that songs with more elements, especially unique elements, and song phrases are more challenging to learn and produce, and that females prefer those songs.

“Song is a cool system in zebra finches, because it’s been used as a model system for understanding human language learning,” Merrill said. “A lot of the ways in which birds learn and process songs are similar to how humans learn and process and produce language.”

In zebra finches, song development occurs in two overlapping stages. From roughly 15 days to 60 days after the birds hatch, they learn songs from older “tutor” males. Then approximately 30 to 90 days after hatching, each bird practices, refines, and crystallizes the song he will sing for life.

Both the volume and connectivity of the brain cells responsible for song learning and production increase around this time in the young bird’s life. The research team hypothesized that stress to the birds’ immune system during this early stage could put those key nuclei at risk, causing the birds to develop less complex songs. That would fit with the concept of selection for “honest signals”—that is, signals that convey information about an individual's underlying genetic, developmental, or epigenetic condition that cannot be cheated.

“In this case, we thought that the region of the brain responsible for this important signal would be sensitive to perturbations because males that experience these challenges in early life probably experience other physiological and somatic changes that make them poorer quality compared to unstressed males,” Merrill said.

However, the team found that male zebra finches who were stressed by KLH early in life grew up to sing more complex songs that contained more elements.

Bird 198 has seven elements in his song (none of which are repeated) and six song phrases.

Bird 295 has 12 elements in his song, but three are repeated for a total of nine unique elements.

And when female zebra finches met the KLH-treated males, they sent more signals of interest (zebra finches “flirt” by hopping and rubbing their beaks on something, like a perch or branch).

“This then begs the question: Do our results mean that for these birds song is no longer an honest signal, or is something else at play?” Merrill said.

In addition to the surprising way early-life stress affected song complexity, the team found negative associations between beak color and song complexity in the birds that received KLH. In other words, the beaks of stressed birds became duller, while song complexity increased.

“This is an area I’ve become really interested in—how early-life experiences influence not just individual traits but the relationship between traits.

“It’s going to require additional work to really begin to uncover and understand the mechanisms responsible for the increased song complexity and the changes to the associations between the two signals,” Merrill said. “On top of that, there are lots and lots of moving parts in play here—the specific type of stressor, the stage of development, and the duration of the stressor, for example. All of these components almost certainly play a role in determining what the short- and long-term outcomes are for an individual.”

The paper “Early-life immune activation increases song complexity and alters phenotypic associations between sexual ornaments” is available online. DOI: 10.1111/1365-2435.12916. Oklahoma State graduate student Madeleine Naylor, University of Illinois graduate student Tara Stewart, and Oklahoma State undergraduate students Merria Dalimonte and Sean McLaughlin also contributed to the research.

This work was supported by a grant from the National Institutes of Health (1R15HD066378-01).